Intracellular Ca²⁺ activates a fast voltage-sensitive K⁺ current in vertebrate sympathetic neurones

Abstract

Many neurones, when depolarized, exhibit two components of outward K⁺ current—the voltage-sensitive delayed rectifier current originally described in squid axons by Hodgkin and Huxley¹, and an additional current triggered by the entry of Ca²⁺ ions². These two currents have been termed I_K and I_C, respectively³. Previous experiments have indicated that both forms of K⁺ current are also present in vertebrate sympathetic neurones^4–6. We have now studied the properties of I_C in bullfrog sympathetic neurones, uncontaminated with I_K, by injecting Ca²⁺ ions into the cells and measuring the resultant outward currents under voltage-clamp, in the manner previously used for large molluscan neurones^7,8. We find three interesting properties of I_C in these vertebrate neurones. First, it shows strong voltage sensitivity independent of the voltage sensitivity of the Ca²⁺ channels (which have been bypassed by the injection technique). Second, I_C activates and deactivates very rapidly (τ_C≤20 ms at 0 mV), with stepped changes in membrane potential. Current fluctuation analysis and patch-clamp records of single-channel currents yielded evidence for appropriate short-lifetime ionic channels with a maximum conductance of ∼100 pS. Finally I_C in ganglion cells is highly sensitive to external tetraethylammonium. We deduce that in these neurones I_C is a fast current which can contribute a substantial fraction to the repolarizing current during an action potential.